NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway

The mechanism by which NQO1 antagonizes PM2.5-induced apoptosis in Sertoli cells through activation of the mitochondrial unfolded protein response (UPRmt) was investigated. A reproductive toxicity model was established using TM4 cells exposed to PM2.5 (50 μg/mL, 24 h). Transcriptome sequencing and b...

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Main Authors: Cao Wang, Qing Xiao, Mingchen Xiao, Yu Chu, Yaya Ai, Zhen Luo, Guangxu Zhou, Kaiyi Mao, Bin Liu
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325010747
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author Cao Wang
Qing Xiao
Mingchen Xiao
Yu Chu
Yaya Ai
Zhen Luo
Guangxu Zhou
Kaiyi Mao
Bin Liu
author_facet Cao Wang
Qing Xiao
Mingchen Xiao
Yu Chu
Yaya Ai
Zhen Luo
Guangxu Zhou
Kaiyi Mao
Bin Liu
author_sort Cao Wang
collection DOAJ
description The mechanism by which NQO1 antagonizes PM2.5-induced apoptosis in Sertoli cells through activation of the mitochondrial unfolded protein response (UPRmt) was investigated. A reproductive toxicity model was established using TM4 cells exposed to PM2.5 (50 μg/mL, 24 h). Transcriptome sequencing and bioinformatics analysis identified NQO1 as the target gene, playing a key role in redox regulation and apoptosis. Phenotypic analysis showed that PM2.5 exposure significantly increased intracellular ROS levels (P < 0.01), induced structural disintegration of mitochondrial cristae (as observed by TEM), and activated apoptosis pathways. Overexpression of NQO1 effectively mitigated these effects. The mechanistic analysis demonstrated that NQO1 overexpression significantly upregulated UPRmt-related proteins (HSP60, ATF5, and CLPP) (P < 0.05), increased SOD activity, and reduced MDA levels (P < 0.01). On the other hand, NQO1 knockout led to mitochondrial membrane potential loss and Cytochrome C release via UPRmt inhibition (P < 0.01), resulting in an increased Bax/Bcl-2 ratio and enhanced apoptosis. Overall, these findings suggest that the NQO1-UPRmt axis protects against PM2.5-induced germ cell damage by maintaining mitochondrial protein homeostasis and redox balance. This study identifies potential therapeutic targets for male infertility associated with environmental pollutants.
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spelling doaj-art-83cd6fea6f284b5a99ccd5c430a92c342025-08-20T04:02:32ZengElsevierEcotoxicology and Environmental Safety0147-65132025-09-0130211872910.1016/j.ecoenv.2025.118729NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathwayCao Wang0Qing Xiao1Mingchen Xiao2Yu Chu3Yaya Ai4Zhen Luo5Guangxu Zhou6Kaiyi Mao7Bin Liu8Department of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou province, China; Guizhou Children's Hospital, Zunyi, Guizhou province, ChinaDepartment of Pediatric Surgery, Longgang District Maternity &amp; Child Healthcare Hospital of Shenzhen City, Shenzhen, Guangdong Province 518100, China; Department of Pediatric Surgery, Longgang Maternity and Child Institute of Shantou University Medical College, Shenzhen, Guangdong Province 518100, China; Corresponding author at: Department of Pediatric Surgery, Longgang District Maternity &amp; Child Healthcare Hospital of Shenzhen City, Shenzhen, Guangdong Province 518100, China.The mechanism by which NQO1 antagonizes PM2.5-induced apoptosis in Sertoli cells through activation of the mitochondrial unfolded protein response (UPRmt) was investigated. A reproductive toxicity model was established using TM4 cells exposed to PM2.5 (50 μg/mL, 24 h). Transcriptome sequencing and bioinformatics analysis identified NQO1 as the target gene, playing a key role in redox regulation and apoptosis. Phenotypic analysis showed that PM2.5 exposure significantly increased intracellular ROS levels (P < 0.01), induced structural disintegration of mitochondrial cristae (as observed by TEM), and activated apoptosis pathways. Overexpression of NQO1 effectively mitigated these effects. The mechanistic analysis demonstrated that NQO1 overexpression significantly upregulated UPRmt-related proteins (HSP60, ATF5, and CLPP) (P < 0.05), increased SOD activity, and reduced MDA levels (P < 0.01). On the other hand, NQO1 knockout led to mitochondrial membrane potential loss and Cytochrome C release via UPRmt inhibition (P < 0.01), resulting in an increased Bax/Bcl-2 ratio and enhanced apoptosis. Overall, these findings suggest that the NQO1-UPRmt axis protects against PM2.5-induced germ cell damage by maintaining mitochondrial protein homeostasis and redox balance. This study identifies potential therapeutic targets for male infertility associated with environmental pollutants.http://www.sciencedirect.com/science/article/pii/S0147651325010747PM2.5NQO1Mitochondrial Unfolded Protein Response (UPRmt)Sertoli cellsApoptosis
spellingShingle Cao Wang
Qing Xiao
Mingchen Xiao
Yu Chu
Yaya Ai
Zhen Luo
Guangxu Zhou
Kaiyi Mao
Bin Liu
NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
Ecotoxicology and Environmental Safety
PM2.5
NQO1
Mitochondrial Unfolded Protein Response (UPRmt)
Sertoli cells
Apoptosis
title NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
title_full NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
title_fullStr NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
title_full_unstemmed NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
title_short NQO1 antagonizes PM2.5-induced apoptosis of Sertoli cells by activating the UPRmt pathway
title_sort nqo1 antagonizes pm2 5 induced apoptosis of sertoli cells by activating the uprmt pathway
topic PM2.5
NQO1
Mitochondrial Unfolded Protein Response (UPRmt)
Sertoli cells
Apoptosis
url http://www.sciencedirect.com/science/article/pii/S0147651325010747
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